A genome-wide investigation of the worldwide invader Sargassum muticum shows high success albeit (almost) no genetic diversity

Abstract

Twenty years of genetic studies of marine invaders have shown that successful invaders are often characterized by native and introduced populations displaying similar levels of genetic diversity. This pattern is presumably due to high propagule pressure and repeated introductions. The opposite pattern is reported in this study of the brown seaweed, Sargassum muticum, an emblematic species for circumglobal invasions. Albeit demonstrating polymorphism in the native range, microsatellites failed to detect any genetic variation over 1,269 individuals sampled from 46 locations over the Pacific-Atlantic introduction range. Single-nucleotide polymorphisms (SNPs) obtained from ddRAD sequencing revealed some genetic variation, but confirmed severe founder events in both the Pacific and Atlantic introduction ranges. Our study thus exemplifies the need for extreme caution in interpreting neutral genetic diversity as a proxy for invasive potential. Our results confirm a previously hypothesized transoceanic secondary introduction from NE Pacific to Europe. However, the SNP panel unexpectedly revealed two additional distinct genetic origins of introductions. Also, conversely to scenarios based on historical records, southern rather than northern NE Pacific populations could have seeded most of the European populations. Finally, the most recently introduced populations showed the lowest selfing rates, suggesting higher levels of recombination might be beneficial at the early stage of the introduction process (i.e., facilitating evolutionary novelties), whereas uniparental reproduction might be favored later in sustainably established populations (i.e., sustaining local adaptation).

Keywords: RAD sequencing; biological invasion; non‐native species; population genomics; seaweed; selfing.

Figure 1

Study areas, sampling localities, and microsatellite genetic diversity of Sargassum muticum. Three geographic areas were sampled: 1) the native range in Asia and 2) two introduction ranges in the NE Pacific and NE Atlantic. All localities were analyzed with 14 microsatellite loci: eight sites in the native range, nine sites in the NE Pacific, and 37 sites in the NE Atlantic. The relative abundance of each of the 60 multi‐locus genotypes in the three areas is indicated. The localities also analyzed with ddRAD sequencing are highlighted by numbers in large black circles. Details about sample size and localities are provided in Table S1

Figure 2

Distribution of Sargassum muticum multi‐locus genotypes (MLGs) obtained with RAD‐seq loci in the introduction ranges. (a) Minimum spanning network on multi‐locus genotypes (MLGs) detected in the introduced ranges, based on the number of pairwise allelic differences between MLGs, with gray shading of branch inversely proportional to the distance between MLGs, and (b) population level distributions of the 14 MLGs found in the southern NE Pacific and NE Atlantic Group 1 (i.e., NE Atlantic excluding populations no.51 (Thau) & 54 (Porto)). Population private haplotypes are colored in black

Figure 3

Principal component analysis (PCA), using the RAD‐seq dataset, showing individuals coordinates on the first two components (a) and on the first and third component (b). Colors refer to different regions and populations

Figure 4

Bayesian clustering analyses (InStruct software, K = 5) in native and introduced ranges of Sargassum muticum, with 8,788 RAD‐seq loci. Each individual is represented by a vertical line divided into colored segments, the length of which indicates the individual's membership fraction to each of K clusters. Individuals are grouped according to their sampling locality. Locality codes correspond to those given in Figure 1 and Table S1